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Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis Bivirgatus)

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Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis Bivirgatus) toxins Article The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus) Daryl C. Yang 1,2,†, Jennifer R. Deuis 3,†, Daniel Dashevsky 2,†, James Dobson 2,†, Timothy N. W. Jackson 2, Andreas Brust 3, Bing Xie 4, Ivan Koludarov 2, Jordan Debono 2, Iwan Hendrikx 2, Wayne C. Hodgson 1, Peter Josh 5, Amanda Nouwens 5, Gregory J. Baillie 3, Timothy J. C. Bruxner 3, Paul F. Alewood 3, Kelvin Kok Peng Lim 6, Nathaniel Frank 7, Irina Vetter 3,8,* and Bryan G. Fry 2,* 1 Department of Pharmacology, Biomedicine Discovery Institute, Monash University, Clayton 3168, Australia; [email protected] (D.C.Y.); [email protected] (W.C.H.) 2 Venom Evolution Lab, School of Biological Sciences, University of Queensland, St. Lucia 4072, Australia; [email protected] (D.D.); [email protected] (J.D.); [email protected] (T.N.W.J.); [email protected] (I.K.); [email protected] (J.D.); [email protected] (I.H.) 3 Institute for Molecular Bioscience, University of Queensland, St. Lucia 4072, Australia; [email protected] (J.R.D.); [email protected] (A.B.); [email protected] (G.J.B.); [email protected] (T.J.C.B.); [email protected] (P.F.A.) 4 Bejing Genomics Institute-Shenzhen, Shenzhen 518083, China; [email protected] 5 School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia 4072, Australia; [email protected] (P.J.); [email protected] (A.N.) 6 Lee Kong Chian Natural History Museum, National University of Singapore, 2 Conservatory Drive, Singapore 117377, Singapore; [email protected] 7 Mtoxins, 1111 Washington ave, Oshkosh, WI 54901, USA; [email protected] 8 School of Pharmacy, University of Queensland, Woolloongabba 4102, Australia * Correspondence: [email protected] (I.V.); [email protected] (B.G.F.); Tel: +61-7-3346-2660 (I.V.); +61-4-0019-3182 (B.G.F.) † These authors contributed equally to this work. Academic Editor: Jan Tygat Received: 15 September 2016; Accepted: 10 October 2016; Published: 18 October 2016 Abstract: Millions of years of evolution have fine-tuned the ability of venom peptides to rapidly incapacitate both prey and potential predators. Toxicofera reptiles are characterized by serous-secreting mandibular or maxillary glands with heightened levels of protein expression. These glands are the core anatomical components of the toxicoferan venom system, which exists in myriad points along an evolutionary continuum. Neofunctionalisation of toxins is facilitated by positive selection at functional hotspots on the ancestral protein and venom proteins have undergone dynamic diversification in helodermatid and varanid lizards as well as advanced snakes. A spectacular point on the venom system continuum is the long-glanded blue coral snake (Calliophis bivirgatus), a specialist feeder that preys on fast moving, venomous snakes which have both a high likelihood of prey escape but also represent significant danger to the predator itself. The maxillary venom glands of C. bivirgatus extend one quarter of the snake’s body length and nestle within the rib cavity. Despite the snake’s notoriety its venom has remained largely unstudied. Here we show that the venom uniquely produces spastic paralysis, in contrast to the flaccid paralysis typically produced by neurotoxic snake venoms. The toxin responsible, which we have called calliotoxin (δ-elapitoxin-Cb1a), is a three-finger toxin (3FTx). Calliotoxin shifts the voltage-dependence of NaV1.4 activation to more hyperpolarised potentials, inhibits inactivation, and produces large ramp currents, consistent with its profound effects on contractile force in an isolated skeletal muscle preparation. Voltage-gated sodium Toxins 2016, 8, 303; doi:10.3390/toxins8100303 www.mdpi.com/journal/toxins Toxins 2016, 8, 303 2 of 21 channels (NaV) are a particularly attractive pharmacological target as they are involved in almost all physiological processes including action potential generation and conduction. Accordingly, venom peptides that interfere with NaV function provide a key defensive and predatory advantage to a range of invertebrate venomous species including cone snails, scorpions, spiders, and anemones. Enhanced activation or delayed inactivation of sodium channels by toxins is associated with the extremely rapid onset of tetanic/excitatory paralysis in envenomed prey animals. A strong selection pressure exists for the evolution of such toxins where there is a high chance of prey escape. However, despite their prevalence in other venomous species, toxins causing delay of sodium channel inhibition have never previously been described in vertebrate venoms. Here we show that NaV modulators, convergent with those of invertebrates, have evolved in the venom of the long-glanded coral snake. Calliotoxin represents a functionally novel class of 3FTx and a structurally novel class of NaV toxins that will provide significant insights into the pharmacology and physiology of NaV. The toxin represents a remarkable case of functional convergence between invertebrate and vertebrate venom systems in response to similar selection pressures. These results underscore the dynamic evolution of the Toxicofera reptile system and reinforces the value of using evolution as a roadmap for biodiscovery. Keywords: toxicofera; venom; evolution; neurotoxin; sodium channel; pharmacology 1. Introduction Squamate reptiles are a research area of great controversy and debate at all levels, including higher order organismal relationships [1]. Traditional frameworks based upon morphology [2–6] were dramatically over-turned by genetic studies which revealed that the morphological plasticity of these animals had obscured their authentic evolutionary relationships [7–16]. While the genetics are now well-resolved, a form of scientific culture-war persists, with some adherents of morphologically based taxonomy not modifying their position in the face of genetic evidence supporting the paradigm shifts [17]. Attempts at reconstructing the evolutionary history by using a combination of morphology, fossils, and genetics resulted in poorly resolved trees [18] that had significantly different frameworks from those reconstructed using only genetic evidence [7–16]. The utilisation of ambiguous morphological characters (which may be arbitrarily scored as divergent or convergent) creates errors relative to the use of non-ambiguous genetic data. Use of such skewed trees results in flawed conclusions when used to reconstruct the evolutionary history not only of the organisms but also their associated venom systems, such as in [17,19]. Another study which examined tissue pattern expressions of toxin and non-toxin homologues in an attempt to cast doubt on the shared ancestry of reptile venom systems was methodologically flawed due to expression values being calculated using replicate averages of values up to nearly 6,000-fold apart, only averaging N = 2 for many of the experiments, and including failed experiments with zero values in N = 3 calculations (Supplementary Tables S5–S9 of [20]). Squamate reptiles are an extremely morphologically plastic clade, where dramatic variations in size and shape [21] may not be an accurate reflection of the organismal genetic relationships [22–24]. One particular clade (Toxicofera) evolved a morphological feature not otherwise described in extant squamates. The basic substrate for the evolution of reptile venom was the exaptation of existing salivary glands in the common ancestor of toxicoferan reptiles (Anguimorpha and Iguania lizards plus snakes), whereby the protein secreting region was increased in size and further segregated from the mucus secreting region [25]. These glands remained in an apparently incipient state in most Iguania except for vertebrate feeding lineages such as Anolis equestris, Pogona sp., and Chlamydosaurus Kingii. In snakes and anguimorph lizards, however, extensive diversification has occurred [19,25–30]. In particular, this key evolutionary innovation under-pinned the explosive diversification of the advanced snakes [10–15,27,30–36]. While initial venom proteins were pre-existing salivary proteins Toxins 2016, 8, 303 3 of 21 that were heightened in expression, such as CRiSP and kallikrein [27,37–39], the promiscuity venom glands share with other secretory tissues allowed for lineage-specific expression of other protein types [20,25–29,40–48] in addition to low-level reversal of expression of venom-gland-derived proteins in other tissues [40]. For many toxin types, particularly those with high disulphide-bond ratios relative to total amino acid content [37], evolutionary selection pressures resulted in neofunctionalisations that produced a myriad of derived activities [41]. As with many other modes of evolution, periodically the venom proteins undergo punctuated molecular evolution, dynamically diversifying into new functional forms early in their evolution, with periods of stasis after that interrupted by further periods of Gouldian punctuated evolution [49–53]. Examples include elapids first arriving in Australia when it was a continent largely devoid of snakes other than slow moving pythons and burrowing blind snakes [54]. Subsequent explosive organismal diversification was paralleled by dramatic shifts in venom chemistry even between populations with minimal organismal genetic variation [55,56]. Venom is a key evolutionary innovation, in myriad lineages, that diversifies in concert with organismal morphological diversification
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